Abstract
SummaryCourtship song is a critical component of male courtship behavior in Drosophila, making the female more receptive to copulation and communicating species-specific information [1–6]. Sex mosaic studies have shown that the sex of certain regions of the central nervous system (CNS) is critical to song production [7]. Our examination of one of these regions, the mesothoracic ganglion (Msg), revealed the coexpression of two sex-determination genes, fruitless (fru) and doublesex (dsx). Because both genes are involved in creating a sexually dimorphic CNS [8, 9] and are necessary for song production [10–13], we investigated the individual contributions of fru and dsx to the specification of a male CNS and song production. We show a novel requirement for dsx in specifying a sexually dimorphic population of fru-expressing neurons in the Msg. Moreover, by using females constitutively expressing the male-specific isoforms of fru (FruM), we show a critical requirement for the male isoform of dsx (DsxM), alongside FruM, in the specification of courtship song. Therefore, although FruM expression is sufficient for the performance of many male-specific behaviors [14], we have shown that without DsxM, the determination of a male-specific CNS and thus a full complement of male behaviors are not realized.
Highlights
Sex mosaic studies have shown that the sex of the central nervous system (CNS) is critical to the performance of these behaviors, suggesting that sex determination in the CNS is required for male sexual behavior in flies [7, 15, 17,18,19,20,21]
A default splice occurs, giving rise to a class of male-specific fru isoforms (FruM proteins) [10, 13, 22,23,24,25] that are expressed in the CNS and peripheral nervous system (PNS) [23, 25,26,27,28] in regions associated with male-specific behaviors
We examined the role of doublesex, another sexdetermination gene, in the specification of male sexual behavior. dsx transcripts undergo sex-specific splicing by Tra, producing male- and female-specific isoforms: DsxM and DsxF, respectively [29, 30]. dsx is responsible for somatic sexual differentiation [15, 31,32,33] and aspects of sex-specific development in the CNS [8]. dsx is expressed in the CNS and is necessary for wild-type courtship song in males [11, 34]
Summary
Given the critical importance of the sex of the ventral ganglia (including the Msg) to song production, the colocalization of FruM and Dsx in this region suggests that sexually dimorphic developmental mechanisms might be operating in the Msg, contributing to the sexspecific nature of courtship song production. Because some dsx-expressing neurons in the Msg are not fru expressing, we examined the axonal morphology of all mnDFMs to eliminate the possibility of sex-specific DFM innervation.
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